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Abstract

Knowledge on symbiotic microorganisms of insects has increased dramatically in recent years, yet relatively little data are available regarding non-pathogenic viruses. Here we studied the virome of the parasitoid wasp Triapitsyn (Hymenoptera: Encyrtidae), a biocontrol agent of mealybugs. By high-throughput sequencing of viral nucleic acids, we revealed three novel viruses, belonging to the families [provisionally termed AnvRV (Anagyrus vladimiri reovirus)], (AnvIFV) and (AnvDV). Phylogenetic analysis further classified AnvRV in the genus , and AnvDV in the genus . The genome of AnvRV comprises 10 distinct genomic segments ranging in length from 1.5 to 4.2 kb, but only two out of the 10 ORFs have a known function. AnvIFV and AnvDV each have one polypeptide ORF, which is typical of iflaviruses but very un-common among dicistroviruses. Five conserved domains were found along both the ORFs of those two viruses. AnvRV was found to be fixed in an population that was obtained from a mass rearing facility, whereas its prevalence in field-collected was ~15 %. Similarly, the prevalence of AnvIFV and AnvDV was much higher in the mass rearing population than in the field population. The presence of AnvDV was positively correlated with the presence of in the same individuals. Transmission electron micrographs of females’ ovaries revealed clusters and viroplasms of reovirus-like particles in follicle cells, suggesting that AnvRV is vertically transmitted from mother to offspring. AnvRV was not detected in the mealybugs, supporting the assumption that this virus is truly associated with the wasps. The possible effects of these viruses on ’s biology, and on biocontrol agents in general, are discussed. Our findings identify RNA viruses as potentially involved in the multitrophic system of mealybugs, their parasitoids and other members of the holobiont.

Funding
This study was supported by the:
  • Israel Science Foundation (Award 397/21)
    • Principle Award Recipient: EinatZchori-Fein
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/content/journal/jgv/10.1099/jgv.0.001810
2022-12-06
2024-04-23
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References

  1. Zchori-Fein E, Bourtzis K. Manipulative Tenants; Bacteria Associated with Arthropods Boca Raton: CRC Press; 2011 [View Article]
    [Google Scholar]
  2. Drew GC, Stevens EJ, King KC. Microbial evolution and transitions along the parasite-mutualist continuum. Nat Rev Microbiol 2021; 19:623–638 [View Article] [PubMed]
    [Google Scholar]
  3. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. Redefining the invertebrate RNA virosphere. Nature 2016; 540:539–543 [View Article]
    [Google Scholar]
  4. Webster CL, Longdon B, Lewis SH, Obbard DJ. Twenty-five new viruses associated with the Drosophilidae (Diptera). Evol Bioinform Online 2016; 12:13–25 [View Article]
    [Google Scholar]
  5. Wu H, Pang R, Cheng T, Xue L, Zeng H et al. Abundant and siverse RNA viruses in insects revealed by RNA-Seq analysis: ecological and evolutionary implications. mSystems 2020; 5:1–14 [View Article]
    [Google Scholar]
  6. Godfray HCJ. Parasitoids: Behavioral and Evolutionary Ecology Princeton University Press; 1994 [View Article]
    [Google Scholar]
  7. Varaldi J, Boulétreau M, Fleury F. Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi. Parasitology 2005; 131:161–168 [View Article] [PubMed]
    [Google Scholar]
  8. Varaldi J, Fouillet P, Ravallec M, López-Ferber M, Boulétreau M et al. Infectious behavior in a parasitoid. Science 2003; 302:1930 [View Article]
    [Google Scholar]
  9. Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J et al. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc Biol Sci 2015; 282:20142773 [View Article]
    [Google Scholar]
  10. Coffman KA, Harrell TC, Burke GR. A mutualistic Poxvirus exhibits convergent evolution with other heritable viruses in parasitoid wasps. J Virol 2020; 94:e02059-19 [View Article]
    [Google Scholar]
  11. Herniou EA, Huguet E, Thézé J, Bézier A, Periquet G et al. When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos Trans R Soc Lond B Biol Sci 2013; 368:20130051 [View Article]
    [Google Scholar]
  12. Bugila AAA, Franco JC, Silva E da, Branco M. Suitability of five mealybug species (Hemiptera: Pseudococcidae) as hosts for the solitary parasitoid Anagyrus sp. nr. pseudococci (girault) (Hymenoptera: Encyrtidae). Biocontrol Sci Technol 2015; 25:108–120 [View Article]
    [Google Scholar]
  13. Studies on an Israel strain of Anagyrus pseudococci (Girault) [Hym., Encyrtidae]. II. Some biological aspects. Entomophaga 1967; 12:111–118 [View Article]
    [Google Scholar]
  14. Izraeli Y, Lalzar M, Mozes-Daube N, Steinberg S, Chiel E et al. Wolbachia influence on the fitness of Anagyrus vladimiri (Hymenoptera: Encyrtidae), a bio-control agent of mealybugs. Pest Manag Sci 2021; 77:1023–1034 [View Article]
    [Google Scholar]
  15. Martinez J, Lepetit D, Ravallec M, Fleury F, Varaldi J. Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects. J Gen Virol 2016; 97:523–535 [View Article] [PubMed]
    [Google Scholar]
  16. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res 2015; 43:D222–6 [View Article] [PubMed]
    [Google Scholar]
  17. IRESite: The database of experimentally verified IRES structures; 2022 http://www.iresite.org/IRESite_web.php?page=blastsearch&search_type=blast_iress
  18. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article]
    [Google Scholar]
  19. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  20. Luria N, Smith E, Lachman O, Laskar O, Sela N et al. Isolation and characterization of a novel cripavirus, the first Dicistroviridae family member infecting the cotton mealybug Phenacoccus solenopsis. Arch Virol 2020; 165:1987–1994 [View Article] [PubMed]
    [Google Scholar]
  21. Khramtsov NV, Woods KM, Nesterenko MV, Dykstra CC, Upton SJ. Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Mol Microbiol 1997; 26:289–300 [View Article] [PubMed]
    [Google Scholar]
  22. Sorrentino S, Carsana A, Furia A, Doskocil J, Libonati M. Ionic control of enzymic degradation of double-stranded RNA. Biochim Biophys Acta 1980; 609:40–52 [View Article]
    [Google Scholar]
  23. Matthijnssens J, Attoui H, Bányai K, Brussaard CPD, Danthi P et al. ICTV virus taxonomy profile: Reoviridae. J Gen Virol 2022; 103: [View Article]
    [Google Scholar]
  24. Cheng RL, Li XF, Zhang CX. Novel Dicistroviruses in an unexpected wide range of invertebrates. Food Environ Virol 2021; 13:423–431 [View Article]
    [Google Scholar]
  25. Shah PNM, Stanifer ML, Höhn K, Engel U, Haselmann U et al. Genome packaging of reovirus is mediated by the scaffolding property of the microtubule network. Cell Microbiol 2017; 19:e12765 [View Article]
    [Google Scholar]
  26. Martinez-Mercado MA, de Jesús JLD, Galindo-Sánchez CE, Saavedra-Flores A, Carrillo-Tripp J. Novel viral RNA genomes of the vine mealybug Planococcus ficus. J Gen Virol 2022; 103: [View Article]
    [Google Scholar]
  27. Wu C-Y, Zhao Y-J, Zhu J-Y. Genome sequence of a novel member of the order Picornavirales from the endoparasitoid wasp Diversinervus elegans. Arch Virol 2021; 166:295–297 [View Article] [PubMed]
    [Google Scholar]
  28. Renault S, Stasiak K, Federici B, Bigot Y. Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J Insect Physiol 2005; 51:137–148 [View Article] [PubMed]
    [Google Scholar]
  29. Graham RI, Rao S, Sait SM, Attoui H, Mertens PPC et al. Sequence analysis of a reovirus isolated from the winter moth Operophtera brumata (Lepidoptera: Geometridae) and its parasitoid wasp Phobocampe tempestiva (Hymenoptera: Ichneumonidae). Virus Res 2008; 135:42–47 [View Article]
    [Google Scholar]
  30. Renault S, Bigot S, Lemesle M, Sizaret P-YY, Bigot Y. The cypovirus Diadromus pulchellus RV-2 is sporadically associated with the endoparasitoid wasp D. pulchellus and modulates the defence mechanisms of pupae of the parasitized leek-moth, Acrolepiopsis assectella. J Gen Virol 2003; 84:1799–1807 [View Article] [PubMed]
    [Google Scholar]
  31. Deacutis J. The characterization and biological effects of a novel cypovirus on the Heliothis virescens and Campoletis sonorensis host-parasitoid system. University of Kentucky; 2012
  32. Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y et al. ICTV virus taxonomy profile: Dicistroviridae. J Gen Virol 2017; 98:355–356 [View Article]
    [Google Scholar]
  33. Zhang J, Wang F, Yuan B, Yang L, Yang Y et al. A novel cripavirus of an ectoparasitoid wasp increases pupal duration and fecundity of the wasp’s Drosophila melanogaster host. ISME J 2021; 15:3239–3257 [View Article]
    [Google Scholar]
  34. Lüthi MN, Vorburger C, Dennis AB. A Novel RNA Virus in the parasitoid wasp Lysiphlebus fabarum: genomic structure, prevalence, and transmission. Viruses 2020; 12:E59 [View Article]
    [Google Scholar]
  35. Perreau J, Moran NA. Genetic innovations in animal-microbe symbioses. Nat Rev Genet 2022; 23:23–39 [View Article] [PubMed]
    [Google Scholar]
  36. Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y et al. ICTV virus taxonomy profile: Iflaviridae. J Gen Virol 2017; 98:527–528 [View Article]
    [Google Scholar]
  37. MacLachlan NJ, Dubovi EJ. Reoviridae. In Fenner’s Veterinary Virology, Fifth Edition. Academic Press; 2017 p 299
    [Google Scholar]
  38. Varaldi J, Gandon S, Rivero A, Patot S, Fleury F et al. A newly discovered virus manipulates superparasitism behavior in A parasitoid wasp. In Bourtzis K, Miller TA. eds Insect Symbiosis Taylor and Francis, Boca Raton, FL: CRC Press; 2006 pp 141–162 [View Article]
    [Google Scholar]
  39. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 2011; 332:254–256 [View Article] [PubMed]
    [Google Scholar]
  40. Perlmutter JI, Bordenstein SR. Microorganisms in the reproductive tissues of arthropods. Nat Rev Microbiol 2020; 18:97–111 [View Article] [PubMed]
    [Google Scholar]
  41. Blumberg D. Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol Control 1997; 8:225–236 [View Article]
    [Google Scholar]
  42. Blumberg D, Klein M, Mendel Z. Response by encapsulation of four mealybug species (Homoptera: Pseudococcidae) to parasitization by Anagyrus pseudococci. Phytoparasitica 1995; 23:157–163 [View Article]
    [Google Scholar]
  43. Suma P, Mansour R, Russo A, La Torre I, Bugila AAA et al. Encapsulation rates of the parasitoid Anagyrus sp. nr. pseudococci, by three mealybug species (Hemiptera: Pseudococcidae). Phytoparasitica 2012; 40:11–16 [View Article]
    [Google Scholar]
  44. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN. Wolbachia and virus protection in insects. Science 2008; 322:702 [View Article]
    [Google Scholar]
  45. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 2011; 476:454–457 [View Article] [PubMed]
    [Google Scholar]
  46. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011; 476:450–453 [View Article]
    [Google Scholar]
  47. Cogni R, Ding SD, Pimentel AC, Day JP, Jiggins FM. Wolbachia reduces virus infection in a natural population of Drosophila. Commun Biol 2021; 4:1327 [View Article]
    [Google Scholar]
  48. Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M et al. The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 2010; 84:9310–9317 [View Article] [PubMed]
    [Google Scholar]
  49. Kliot A, Cilia M, Czosnek H, Ghanim M. Implication of the bacterial endosymbiont Rickettsia spp. in interactions of the whitefly Bemisia tabaci with tomato yellow leaf curl virus. J Virol 2014; 88:5652–5660 [View Article] [PubMed]
    [Google Scholar]
  50. Bonning BC, Miller WA. Dicistroviruses. Annu Rev Entomol 2010; 55:129–150 [View Article]
    [Google Scholar]
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